Florida's Harmful Algal Bloom (HAB) Problem: Escalating Risks to Human, Environmental and Economic Health With Climate Change - Frontiers
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REVIEW
published: 17 June 2021
doi: 10.3389/fevo.2021.646080
Florida’s Harmful Algal Bloom (HAB)
Problem: Escalating Risks to Human,
Environmental and Economic Health
With Climate Change
Cynthia Ann Heil 1* and Amanda Lorraine Muni-Morgan 1,2
1
Mote Marine Laboratory & Aquarium, Sarasota, FL, United States, 2 Soil and Water Quality Laboratory, Gulf Coast Research
and Education Center, Institute of Food and Agricultural Sciences, University of Florida, Wimauma, FL, United States
Harmful Algal Blooms (HABs) pose unique risks to the citizens, stakeholders, visitors,
environment and economy of the state of Florida. Florida has been historically subjected
to reoccurring blooms of the toxic marine dinoflagellate Karenia brevis (C. C. Davis)
G. Hansen & Moestrup since at least first contact with explorers in the 1500’s.
However, ongoing immigration of more than 100,000 people year−1 into the state,
elevated population densities in coastal areas with attendant rapid, often unregulated
Edited by: development, coastal eutrophication, and climate change impacts (e.g., increasing
Frank S. Gilliam, hurricane severity, increases in water temperature, ocean acidification and sea level
University of West Florida,
United States rise) has likely increased the occurrence of other HABs, both freshwater and marine,
Reviewed by: within the state as well as the number of people impacted by these blooms. Currently,
Albertus J. Smit, over 75 freshwater, estuarine, coastal and marine HAB species are routinely monitored
University of the Western Cape,
South Africa
by state agencies. While only blooms of K. brevis, the dinoflagellate Pyrodinium
H. Dail Laughinghouse IV, bahamense (Böhm) Steidinger, Tester, and Taylor and the diatom Pseudo-nitzschia spp.
University of Florida, United States have resulted in closure of commercial shellfish beds, other HAB species, including
*Correspondence: freshwater and marine cyanobacteria, pose either imminent or unknown risks to
Cynthia Ann Heil
cheil@mote.org human, environmental and economic health. HAB related human health risks can
be classified into those related to consumption of contaminated shellfish and finfish,
Specialty section:
consumption of or contact with bloom or toxin contaminated water or exposure to
This article was submitted to
Biogeography and Macroecology, aerosolized HAB toxins. While acute human illnesses resulting from consumption of
a section of the journal brevetoxin-, saxitoxin-, and domoic acid-contaminated commercial shellfish have been
Frontiers in Ecology and Evolution
minimized by effective monitoring and regulation, illnesses due to unregulated toxin
Received: 24 December 2020
Accepted: 22 April 2021
exposures, e.g., ciguatoxins and cyanotoxins, are not well documented or understood.
Published: 17 June 2021 Aerosolized HAB toxins potentially impact the largest number of people within Florida.
Citation: While short-term (days to weeks) impacts of aerosolized brevetoxin exposure are
Heil CA and Muni-Morgan AL
well documented (e.g., decreased respiratory function for at-risk subgroups such as
(2021) Florida’s Harmful Algal Bloom
(HAB) Problem: Escalating Risks asthmatics), little is known of longer term (>1 month) impacts of exposure or the
to Human, Environmental risks posed by aerosolized cyanotoxin [e.g., microcystin, β-N-methylamino-L-alanine
and Economic Health With Climate
Change. Front. Ecol. Evol. 9:646080.
(BMAA)] exposure. Environmental risks of K. brevis blooms are the best studied of
doi: 10.3389/fevo.2021.646080 Florida HABs and include acute exposure impacts such as significant dies-offs of fish,
Frontiers in Ecology and Evolution | www.frontiersin.org 1 June 2021 | Volume 9 | Article 646080Heil and Muni-Morgan Escalating HAB Risks in Florida
marine mammals, seabirds and turtles, as well as negative impacts on larval and juvenile
stages of many biota. When K. brevis blooms are present, brevetoxins can be found
throughout the water column and are widespread in both pelagic and benthic biota.
The presence of brevetoxins in living tissue of both fish and marine mammals suggests
that food web transfer of these toxins is occurring, resulting in toxin transport beyond
the spatial and temporal range of the bloom such that impacts of these toxins may
occur in areas not regularly subjected to blooms. Climate change impacts, including
temperature effects on cell metabolism, shifting ocean circulation patterns and changes
in HAB species range and bloom duration, may exacerbate these dynamics. Secondary
HAB related environmental impacts are also possible due to hypoxia and anoxia resulting
from elevated bloom biomass and/or the decomposition of HAB related mortalities.
Economic risks related to HABs in Florida are diverse and impact multiple stakeholder
groups. Direct costs related to human health impacts (e.g., increased hospital visits) as
well as recreational and commercial fisheries can be significant, especially with wide-
spread sustained HABs. Recreational and tourism-based industries which sustain a
significant portion of Florida’s economy are especially vulnerable to both direct (e.g.,
declines in coastal hotel occupancy rates and restaurant and recreational users) and
indirect (e.g., negative publicity impacts, associated job losses) impacts from HABs.
While risks related to K. brevis blooms are established, Florida also remains susceptible
to future HABs due to large scale freshwater management practices, degrading water
quality, potential transport of HABs between freshwater and marine systems and the
state’s vulnerability to climate change impacts.
Keywords: HAB, Florida, Karenia brevis, climate change, risks, toxins
INTRODUCTION a bloom is also highly variable. Smayda (1997) argues that
biomass alone is insufficient to describe a bloom as harmful
Phytoplankton, the microscopic algae found in freshwater, and that the environmental consequences of a bloom must be
estuarine and marine waters, are critically important to both considered. A smaller subset of these HABs, ∼2% of total species
human and the planet’s health. They form the basis of aquatic (Sournia, 1995; Knap et al., 2002), produce secondary metabolites
food webs, and thus are essential for the secondary production which can be toxic or fatal. Although the majority of toxic
of shellfish and finfish that provide ∼16% of the world’s HAB species are Dinophyceae, species of Bacillariophyceae and
protein supply (Cato, 1998). They are responsible for ∼50% Raphidophyceae, some Prasinophyceae as well as photosynthetic
of global photosynthesis (Longhurst et al., 1995; Field et al., bacteria (Cyanophyceae/Cyanobacteria) can be toxic.
1998; Beardall et al., 2009), producing between 50–85% of the Within the past 30 years, there has been increasing scientific
O2 in the atmosphere. Their role in sequestering atmospheric and public focus on and concern about HABs for several
CO2 through photosynthesis and transferring this carbon (C) reasons. In the late 1980’s and early 1990’s, a trend of
to ocean sediments is considered a major buffer of climate increasing frequency, geographical distribution and abundance
change impacts (Falkowski, 2012). A small subset of the estimated of some HAB species, primarily dinoflagellates, was recognized
5,000 (Sournia et al., 1991; Sournia, 1995; Tett and Barton, (Anderson, 1989; Maclean, 1989; Smayda, 1989, 1990). These
1995) to 100,000 (Round and Crawford, 1984) phytoplankton trends have increasingly been documented for additional species
species in the ocean form blooms, an accumulation of cells of and groups (e.g., Cyanophyceae, Paerl and Paul, 2012; Harke
one or more species that occurs through physical concentration et al., 2016) in subsequent years (Chinain et al., 2020a; Yñiguez
and/or in situ cell growth, with approximately 300 species et al., 2020; Anderson et al., 2021), and HABs are now an almost
involved in harmful bloom events (Berdalet et al., 2016). routine occurrence among much of the world’s coastal waters.
Blooms are considered to be a harmful algal bloom (HAB) HAB increases are attributed to a variety of reasons that vary with
when they become harmful to human, ecosystem or economic the species and the geographical areas involved (Anderson, 1989;
health. Harmful is a broad term, however, and can include Hallegraeff, 1993; Burkholder, 1998; Glibert et al., 2005; Glibert
both direct (e.g., damage due to cell morphology, toxins or and Burkholder, 2006). These include increasing coastal nutrient
other substances) and indirect (e.g., O2 depletion due to inputs and eutrophication, coastal development, industrial and
respiratory demands of high biomass) impacts of cells. The agricultural intensification (Smayda, 1990; Anderson et al., 2002,
concentration of cells of an individual species that constitutes 2008; Glibert et al., 2006; Heisler et al., 2008; Glibert, 2020),
Frontiers in Ecology and Evolution | www.frontiersin.org 2 June 2021 | Volume 9 | Article 646080Heil and Muni-Morgan Escalating HAB Risks in Florida ballast water transport (Hallegraeff and Gollasch, 2006; Doblin environmental conditions, from marine lagoonal systems with et al., 2007; Smayda, 2007), increases in shellfish aquaculture restricted flows and residence times (e.g., the Indian River (Shumway, 2011), climate change (Dale et al., 2006; Moore Lagoon, Florida Bay) to a north flowing river (e.g., St Johns et al., 2008; Hallegraeff, 2010; O’Neil et al., 2012; Gobler, River), to classical river driven estuaries (e.g., Charlotte Harbor 2020) and a potential observer effect. In most cases, there is and Apalachicola Bay). There are more than 7,800 lakes probably not a single cause underlying increases in a HAB’s in Florida (Brenner et al., 1990), including the 4th largest frequency, distribution or toxicity, but rather a complex interplay United States natural lake, the 488,000-acre Lake Okeechobee, between these external pressures and the unique physiology of and numerous freshwater springs. The natural geology of the HAB species involved which allows it to dominate under Florida also plays a role in the prevalence of HABs. The certain conditions. sandstone and permeable limestone that characterize Florida Florida is arguably one of the global epicenters of HABs. karst topography produce a soil characterized by relatively Harmful and toxic micro- and macroalgal and cyanobacterial poor nutrient retention (Slomp and Van Cappellen, 2004), species are found in all of Florida’s aquatic environments, which likely contributes to coastal eutrophication. The central from freshwater springs and lakes, to coastal lagoons, estuaries west Florida region is also characterized by the Hawthorne and shelf waters. Three algal toxins, brevetoxin, saxitoxin and Phosphatic Deposits, a natural phosphorus (P) rich geological domoic acid, have been detected in state waters, resulting in feature that has been mined continually since the late 19th regulatory actions, including shellfish bed closures. One of the century (Filippelli, 2011) and results in elevated inorganic and most predictable of global HABs, blooms of K. brevis, occur organic P concentrations in central and southwest Florida coastal almost annually between August and November in southwest waters (Heil et al., 2007). Florida experiences a wide range of Florida coastal waters (Steidinger, 2009). These blooms are climate, from the warm temperate climate of the Panhandle to the cause of both neurotoxic shellfish poisoning (NSP) and the Florida Keys, which constitute the northern boundary of respiratory irritation (Table 1) and are the focus of intensive the tropics. Florida’s weather systems are characterized by two state monitoring and management (Heil and Steidinger, 2009). seasons, a wet season and a dry season, which can exacerbate Several Florida coastal regions (Indian River Lagoon, Tampa Bay, nutrient retention and runoff conditions seasonally. Multiple Charlotte Harbor) are also subject to blooms of the dinoflagellate anthropogenic stressors act on these diverse natural systems Pyrodinium bahamense, which can contain saxitoxins that are on different scales. Florida’s human population is constantly responsible for both paralytic shellfish poisoning (PSP) and increasing, an estimated 845 people move to Florida each day saxitoxin puffer fish poisoning (SPFP) (Landsberg et al., 2006; (Office of Economic and Demographic Research, 2021). In south Abbott et al., 2009). The detection of domoic acid, a toxic, water Florida alone, population is projected to increase to over ten soluble (Falk et al., 1991) amino acid produced by some species million by 2025 and possibly 15 million by 2050 (Obeysekera in the diatom genus Pseudo-nitzschia, has resulted in shellfish et al., 2011). Population increases have been accompanied by closures in St. Joseph Bay, Florida for the first time in 2013 rapid, often unregulated, residential development. Urban and and thereafter in 2014 and 2017 (O’Dea et al., 2013; Hubbard agricultural development and other associated anthropogenic et al., 2015, 2017). Cyanobacterial toxins (e.g., microcystins activities lead to increasing water demands as well as stormwater, and cylindrospermopsins) have also been detected in Florida wastewater, and agricultural runoff to inland and coastal aquatic fresh (Williams et al., 2007) and marine (Metcalf et al., 2021) systems. In Florida, coastal development has been ongoing waters at concentrations within EPA Drinking Water Health since 1912 when the Florida East Coast Railway linked to Advisory (HA) levels (United States Environmental Protection the Florida Keys, and has been characterized by both recent Agency, 2015). Other harmful blooms also occur with either and historical marine and freshwater eutrophication (Brezonik uncharacterized toxins (e.g., undescribed Karenia species) or et al., 1969; Lapointe and Clark, 1992; Havens and James, biomass related impacts [e.g., Synechococcus sp. blooms in Florida 2005; Turner et al., 2006; Barile, 2018; Lapointe et al., 2019, Bay (Glibert et al., 2009b,c, 2021), and Aureoumbra lagunensis 2020). An additional anthropogenic activity in Florida is the D. A. Stockwell, DeYoe, Hargraves & P. W. Johnson blooms management of freshwater flows by both state and federal levels. in the Indian River Lagoon (Gobler et al., 2013; Kang et al., Lake Okeechobee water levels are managed by the United States 2015)]. Army Corps of Engineers for human safety (Steinman et al., Why are HABs so prevalent in Florida waters? There is 2002), which in 2018 resulted in the release of Microcystis no single explanation. Indeed, a number of unique biological, contaminated lake waters to both the eastern coast via the chemical and physical drivers as well as local, regional and global St. Lucie River and the west coast by the Caloosahatchee stressors are likely contributing to Florida’s HAB prevalence, all River (Krimsky et al., 2018). Indeed, South Florida is currently of which may be occurring at different temporal and spatial undergoing one of the largest flow restoration projects in the scales. There are numerous freshwater, estuarine and marine world, the Comprehensive Everglades Restoration Plan (CERP), potential HAB habitats available. Florida has a long coastline, which is impacting the amount, timing and distribution of 2,170 km, second only to Alaska in terms of length. This freshwater flows and subsequent nutrient loading to the southern coastline borders two bodies of water, the Atlantic Ocean third of the state (Glibert et al., 2021). Overlying these natural and the Gulf of Mexico (GoM) and is easily accessible from features and anthropogenic stressors are the escalating effects within 175 miles of any position within the state. Florida’s of climate change. Florida is considered especially susceptible coastal environments are characterized by widely varying to the effects of climate change, from warming waters to sea Frontiers in Ecology and Evolution | www.frontiersin.org 3 June 2021 | Volume 9 | Article 646080
Heil and Muni-Morgan Escalating HAB Risks in Florida
TABLE 1 | HAB Syndromes and associated marine HAB species and toxins reported from Florida.
Syndrome Toxin Species Vector Regulatory level Mode of action
Neurotoxic shellfish Brevetoxins Karenia brevis Shellfish, water =0.8 mg/kg [20 mouse Voltage dependent Na
poisoning (NSP) units (MU)/100 g] channel, Site 5
brevetoxin-2 equivalent
or 5,000 cells/L
Paralytic shellfish Saxitoxin and Pyrodinium bahamense Shellfish =0.8 mg/kg saxitoxin Voltage dependent Na
poisoning (PSP) derivatives var. bahamense equivalents channel, Site 1
(80 mg/100 gm)
Amnesic shellfish Domoic acid and Psuedo-nitzschia spp. Fish, shellfish, =20 mg/kg domoic Glutamate receptors
poisoning (ASP) isomers crustaceans acid
Saxitoxin puffer fish Saxitoxin and Pyrodinium bahamense Fish =0.8 mg/kg saxitoxin Voltage dependent Na
poisoning (SPFP) derivatives var. bahamense equivalents channel, Site 1
(80 mg/100 gm)
Ciguatera fish Ciguatoxins Gambierdiscus toxicus Reef fish Caribbean ciguatoxins: Voltage dependent Na
poisoning (CFP) >0.1 mg/kg Caribbean channel, Site 5
Ciguatoxins-1
(C-CTX-1) equivalents
Diarrheic shellfish Okadaic acid and Dinophysis spp. Shellfish =0.16 mg/kg okadaic Serine/threonine
poisoning (DSP) derivatives Prorocentrum spp. acid equivalents protein phosphatases
level rise to increasing storm intensities (Obeysekera et al., 2011; depending on the particular HAB species, the toxin involved and
Reece et al., 2013). the route of exposure (Berdalet et al., 2016). Global estimates of
Harmful Algal Blooms and their associated toxins thus HAB related human intoxification incidences range from 6,000
represent significant risks to human and environmental health per year (Hallegraeff, 1993; Van Dolah, 2000) to more than
as well as local and state economies within Florida in ways that 500,000 per year (Quod and Turquet, 1996).
are unique to the state. The goal of this review is to provide an These routes of HAB exposure to humans vary with the species
overview of major HAB species of specific concern in Florida involved, the toxin, and even the location, but all fall into one
waters, including a brief review of the ecology and associated of three exposure routes: (1) ingestion of contaminated fish,
risks of these species, and an evaluation of the potential impacts shellfish or drinking water, (2) exposure to aerosolized HAB
of climate change on these species and their associated risks in toxins, or (3) dermal contact with a HAB. All of the human health
the future. As such, it is structured to include an overview of syndromes associated with HAB exposure in Florida (Table 1)
the human, environmental and economic risks associated with result from one of these three routes. Regulatory effects have
HABs in Florida, followed by a review of the different HAB primarily focused on the ingestion route, particularly that of
groups and major species, then a discussion of the potential shellfish, which through feeding efforts can act to biomagnify
impacts of climate change on these HAB species and future toxins in their tissues. The three toxins that are the primary focus
challenges posed for HAB research and management by these of HAB monitoring in Florida, brevetoxin, saxitoxin, and domoic
impacts. How climate change is impacting HABs now and in acid, all have regulatory levels established by the FDA [FDA and
the future in Florida represents a major challenge for local, EPA Safety Levels in Regulations and Guidance, A5 – 12 (March
state and federal HAB researchers and managers. By highlighting 2020)]. This is because the risks associated with ingestion of
the ecology and impacts of the major HABs and the potential these toxins are most closely defined by the formal framework
impacts of the local (e.g., water quality), regional and global for Risk Assessment outlined by the National Research Council
stressors (e.g., climate change) on Florida’s HABs, our hope is to in 1983 (National Research Council [NRC], 1983), which include
provide potential direction on relevant future research efforts to 4 sequential steps: (1) identification of the hazard, (2) a dose-
reduce these risks. response assessment of the hazard, (3) exposure assessment of
the hazard, and (4) a risk characterization of human exposure.
Brevetoxin, saxitoxin and domoic acid have been identified
HAB ASSOCIATED RISKS and chemically characterized and the dose required for impacts
has been estimated from natural events and epidemiological
The impacts of HABs fall into three categories: harmful studies. Exposure assessment establishes the extent and routes
effects upon human health, detrimental environmental impacts of potential toxin exposures, namely ingestion, inhalation or
including impacts to aquatic biota, and economic losses to a range dermal contact. Effect risk characterization merges the last 2 steps
of sectors and stakeholders. Of these three, the assessment of risks to determine the probability of toxin exposure in sufficiently
associated with HABS has focused primarily on human health high concentrations to have a clinical effect (Van Dolah et al.,
(Hitzfeld et al., 2000; Carmichael, 2001; Van Dolah et al., 2001; 2001; Krahl, 2009). This is most easily assessed for ingestion
Krahl, 2009; Cheung et al., 2013; Ibelings et al., 2014; Janssen, of identified toxins. For the majority of HAB species, however,
2019). These effects can be significant, even life threatening, the information required to assess risk, from identification of
Frontiers in Ecology and Evolution | www.frontiersin.org 4 June 2021 | Volume 9 | Article 646080Heil and Muni-Morgan Escalating HAB Risks in Florida
the toxin and its chemical structure to determining potential year (United Nations Environment Programme, Joint Group
biomarkers of exposure is poorly understood or unknown. Thus, of Experts on the Scientific Aspects of Marine Environmental
the assessment of human risk associated with most HABs is Protection, 2001, references in Berdalet et al., 2016). Estimates
in its early stages, especially for inhalation and dermal contact of HAB related losses in the United States have been steadily
exposure routes. increasing over time. Anderson et al. (2000) and Hoagland et al.
Health risk assessment of HABS is further hampered by (2002) put annual losses related to HABs in the United States
many additional factors, including a lack of toxin identification at $20 million dollars at the start of the 21st century. These
for some species as well as lack of knowledge of toxin estimates have increased from $50 to $82 million dollars annually
transformations in the environment, lack of biomarkers of (Hoagland and Scatasta, 2006; Anderson et al., 2012). These
exposure, and even the dynamic physical nature of blooms economic costs generally are attributed to losses in four sectors:
which makes both predicting and determining exposure difficult. public health, commercial fisheries, tourism and recreation, and
Determination of the human health impacts of HAB toxin HAB monitoring and management. They include economic
exposure has largely focused on acute impacts of limited losses from relevant markets (e.g., seafood, labor, and coastal
exposure. In Florida, there is a large emphasis on brevetoxins tourism), costs associated with the HAB and its impacts (e.g.,
associated with K. brevis blooms due to frequency and the public health) and the cost of mitigating these impacts (e.g., costs
number of individuals impacted (e.g., Kirkpatrick et al., 2004; of cleaning dead fish from beaches, monitoring) (Hoagland and
Fleming et al., 2011). For many HAB routes of exposure, Scatasta, 2006). Losses attributed to each of these sectors will vary
the health effects of chronic exposure are unknown and greatly with the HAB involved and its impacts.
require further research. For example, the impacts of short- Quantifying the economic risks of HABs and HAB associated
term inhalation of aerosolized brevetoxins from K. brevis blooms losses has proven to be challenging. One difficulty in evaluating
is established (Backer et al., 2003; Fleming et al., 2007, see HAB economic risks lies in their differences from other natural
Fleming et al., 2011 for review). Blooms of K. brevis may persist hazards. HABs differ from other large natural hazards such as
in southwest coastal waters for periods of up to 30 months hurricanes or earthquakes in that their impacts are not necessarily
(Steidinger, 2009) and the impacts of this longer term exposure immediate (Bechard, 2020b) or restricted to a limited area.
of aerosolized brevetoxins are unknown. Even less is known HABs can last for an extended period. The longest duration
about both the acute and chronic impacts of exposure to K. brevis bloom occurred for 30 months from 1994 to 1997
aerosolized cyanotoxins. Increases in the frequency of blooms (FWRI HAB Historical Database) while blooms of Synechococcus
of the toxic cyanobacteria Microcystis in Lake Okeechobee have persisted intermittently in Florida Bay since 1999 for
(Havens and Steinman, 2015; Havens et al., 2019), especially periods of up to 3 years (Glibert et al., 2009b,c). HABs can also
in 2018 when a large Microcystis bloom in the Lake was impact large regions: the 1986–1987 K. brevis bloom impacted
transported to the east and west coasts via release through most of the coastline of Florida and the eastern seaboard as
the St. Lucie and Caloosahatchee Rivers, combined with the far north as North Carolina (Tester et al., 1991; Tester and
detection of microcystin in nasal swabs from people exposed to Steidinger, 1997). Economic impact estimates rarely account
this Microcystis bloom (Schaefer et al., 2020), suggests that this for economic ‘halo’ effects, which are collateral losses resulting
toxin route merits further investigation. from human perceptions related to HABs, such as consumer
The environmental impacts of Florida HABs are diverse and avoidance of goods (e.g., shellfish) perceived as tainted by HAB
significant. Reviews of the impacts of HABs on biota and the toxins (Jensen, 1975; Kuhar et al., 2009; Adams et al., 2018).
environment are provided by Landsberg (2002); Landsberg et al. This can be a significant risk for sectors such as Florida’s tourism
(2009), Basti et al. (2018); Shumway et al. (2018), Zohdi and industry, which relies upon images of pristine beaches to draw
Abbaspour (2019), and Brown et al. (2020). Impacts range from people globally and are heavily impacted by public perception
direct, acute impacts of toxins on freshwater and marine biota (Kuhar et al., 2009; Cahyanto and Liu-Lastres, 2020). This social
(e.g., fish, marine mammal and sea turtle mortalities) to indirect amplification of risk, which may potentially be intensified by the
effects through food web transfer of toxins (Landsberg, 2002; media (Li et al., 2015), is an extensive problem with Florida red
Landsberg et al., 2009) and/or bloom-associated anoxia such as tide specifically (Hoagland et al., 2020).
occurred with larger K. brevis blooms on the central west Florida Within both the United States and Florida, the scientific focus
shelf in 1974 (Smith, 1975, 1979) and 2005 (Hu et al., 2006). of assessing economic losses related to HABs has been primarily
The HAB species and toxins involved are especially important on K. brevis blooms. Adams et al. (2018) in their review of
in predicting environmental impacts associated with blooms. existing literature, research methods, data, and information gaps
In many cases, e.g., K. brevis blooms, acute bloom impacts of current HAB-economic research, point out that 18 of the
are well documented, while routes of toxin transfer are still 36 relevant HAB economic papers focus on K. brevis blooms
being elucidated (Abraham et al., 2021). In other cases, e.g., in Florida. This is not unexpected as K. brevis blooms reoccur
other Karenia species, these impacts are yet to be determined. annually, generally impact larger areas of the state relative
Sublethal impacts, especially during extended blooms, are to other HABs and affect the greatest number of people and
poorly understood and are dependent on our identification and businesses. Initial estimates of economic losses associated with
understanding of the toxin(s) involved, including their structures these blooms range from $20 million dollars for a 1971 bloom
and modes of action. in southwest Florida (Habas and Gilbert, 1974) to $18.45 million
Harmful Algal Blooms are costly. Global estimates of HAB dollars for a 2000 Texas K. brevis bloom (Evans and Jones, 2001).
impacts on human health alone are over $4 billion dollars per Interestingly, Habas and Gilbert (1974) suggest that their estimate
Frontiers in Ecology and Evolution | www.frontiersin.org 5 June 2021 | Volume 9 | Article 646080Heil and Muni-Morgan Escalating HAB Risks in Florida
is likely a significant underestimate of true bloom costs due red tide but suggested this may reflect inadequate data resolution
to an array of costs that were masked by substantial economic or the selection of alternative entertainment by business patrons.
growth during the bloom period. These studies focused primarily Bechard (2019) reported a 15% decrease in sales in Sarasota
on losses within the fisheries and tourism sectors. It is now County during persistent blooms, while the food and restaurant
understood that the economic impacts of these blooms, especially sector losses averaged 1.75%. Similar reductions in adjacent,
the infrequent, longer duration, high impact K. brevis blooms unimpacted counties were not evident. Further research over
such as occurred in 2017–2019, are complex, diverse, and long- an extended 6 county area from Pinellas to Collier Counties in
lasting. Direct economic losses via negatively impacted businesses southwest Florida (Bechard, 2020d) reported that each additional
are predominantly marine (e.g., fisheries and aquatic dependent day of red tide per month in excess of 17 days drove lodging
businesses) or tourism related, and costs to local governments sales down 1–2% and restaurant sales down 0.5–1%. While these
associated with bloom mitigation costs. But significant losses results suggest that economic impacts may be localized to the
are also associated with the costs of bloom associated human areas of the bloom, they also demonstrate that these impacts
health care as well as impacts on property values and government can be significant.
revenues (Adams et al., 2018). Health care costs during K. brevis blooms are related to
Other bloom associated economic losses include losses to digestive, gastrointestinal and respiratory impacts (Hoagland
the fishery (both wild harvest and aquaculture) and seafood et al., 2014; Patel et al., 2020). Kirkpatrick et al. (2006) utilized
sectors. Anderson et al. (2000) estimated that 37% of HAB hospital records to compare the number of patients admitted
related economic losses were attributable to commercial fisheries with respiratory disease during red tide periods with non-bloom
in the United States, which Hoagland and Scatasta (2006) periods and found a significant increase in the ER admissions
increased to 48%. These are likely underestimates as they account for respiratory diseases during the 2001 red tide compared
primarily for direct economic losses and do not include the halo to the 2002 non-red tide period, with elevated rates among
effect (Hoagland and Scatasta, 2006). Béchard (2020a) found individuals living within 1.6 miles of the shore. A 40% increase
that in one Florida County alone, taxable sales receipts for in gastrointestinal diagnoses and admissions were also found
the fishery and seafood sectors experienced a $20,000 monthly (Kirkpatrick et al., 2010). Hoagland et al. (2009) estimated the
loss, or 4.8% below normal, when a K. brevis bloom was costs of respiratory illness associated with K. brevis blooms
present. These estimates also represent ‘acute’ impacts during in Sarasota County alone to be between $0.5 and $4 million
the time of the bloom, generally when extensive fish kills occur. depending on bloom severity. Increased health costs were
Blooms of K. brevis have recently been shown to impact fish associated with older cohorts (>55 years of age) in 6 southwest
community diversity for extended periods (Gannon et al., 2009; Florida counties and ranged from $60,000 to $700,000 annually
DiLeone and Ainsworth, 2019), with severe blooms such as depending on bloom severity (Hoagland et al., 2014). The authors
occurred in 2005 and 2018 resulting in declines in annual suggest that capitalized costs of future K. brevis related illnesses
recruitment of commercially important species such juvenile could be up to $24 million dollars.
spotted seatrout (Cynoscion nebulosus), sand seatrout (Cynoscion Although they reoccur each year, Florida red tides vary greatly
arenarius), and red drum (Sciaenops ocellatus) (Flaherty and in their severity, duration, impacts and spatial extent. The 2017–
Landsberg, 2011), and multiyear closures of some commercial 2019 K. brevis bloom was especially severe, lasting for 17 months
fisheries that are especially sensitive to brevetoxin impacts [e.g., and impacting most of Florida’s 23 Gulf counties. This bloom has
snook (Centropomus undecimalis)], red drum and sea trout provided an opportunity to estimate the higher end economic
(Gillis, Feb 19, 2020). impacts possible with a severe K. brevis bloom. A Gulf of Mexico
Florida’s economy is heavily dependent upon tourism revenue. Alliance Report (The Balmoral Group., 2020) documented the
In 2017–2018 alone, visitors to Florida accounted for from $1.84 total losses attributable to this bloom in Florida Gulf counties
billion dollars economic impact (Visit Sarasota County, 2019) of $1 billion dollars, with an additional tax revenue decline of
to $22 billion dollars in beach related tourism. Much of the $178 million dollars. The tourism sector had by far the greatest
attractiveness of Florida to tourists results from its environment, loss, $455 million dollars in direct loss and a $113 million dollar
including warm weather and a long coastline with beautiful loss in tax revenue, followed by property values ($343 and $32
beaches and a healthy ocean. Any threat to Florida’s environment million dollars, respectively) then boat sales ($55 and $21 million
is a threat to its tourism industry. As such, the economic losses dollars, respectively) and recreational and commercial fisheries.
due to tourism from HABs can be considerable (Habas and Economic losses attributable to human health impacts were not
Gilbert, 1974; Adams et al., 2002; Larkin and Adams, 2007; figured into these losses, nor were losses attributed to marine
Morgan et al., 2009, 2010). Larkin and Adams (2007) report mammal strandings ($198 million dollars, The Balmoral Group.,
reductions in monthly revenue of restaurants and lodging of 2020). Bechard (2019) reported monthly losses to lodging and
$2.8 and $3.7 million dollars, respectively (29 and 35% declines, restaurant sectors to be between 1 and 15% and 0.5 and 1.7%,
respectively) in Ft. Walton Beach and Destin areas of the Florida respectively, during the 2006 and 2018 blooms in counties where
Panhandle for 1995–1997 when a K. brevis bloom was present. red tide was present. Property values within 1 mile of the coast
Three beachfront restaurants reported reductions in revenue due sold for up to 30% less compared with similar homes in areas with
to red tide from $646 to $3,734 (13.7–51.3% on average) per no red tide, and (Bechard, 2021; Bechard, 2020c) reported that
day (Morgan et al., 2009). Adams et al. (2000) was unable to during a 16 year period that included the 2018 bloom, property
demonstrate a negative effect upon beach attendance during a values decreased by 10% during the bloom with an additional
Frontiers in Ecology and Evolution | www.frontiersin.org 6 June 2021 | Volume 9 | Article 646080Heil and Muni-Morgan Escalating HAB Risks in Florida decline of 1–2% for each additional bloom month, with steeper Navy send planes to bomb the dead fish and Rear Admiral decreases experienced by waterfront homes. Davidson telegraphed Senator Pepper that this was ‘inadvisable Little is known of the economic costs associated with as likely to disperse present concentration and involve additional HABs other than K. brevis in Florida. Hoagland and Scatasta beach communities’ (Sarasota Herald Tribune, 1947). Subsequent (2006) attributed public health costs of $250,000 and $525,000 collaborative state and federal efforts focused on the use of copper per year for reported and unreported cases of ciguatera sulfate to control K. brevis blooms in the 1950’s (see Sengco, poisoning, respectively, in Florida from 1987 to 1992. Todd 2009b for review) with additional research on potential algicidal (1985) quantified the economic losses resulting from ciguatera control (Mayali and Doucette, 2002; Roth et al., 2007, 2008; poisoning (medical costs and lost labor) at $2.7 million dollars per Lin et al., 2016; Kinley-Baird et al., 2021) and clay flocculation year, suggesting that Florida’s costs are potentially greater than thereafter (Sengco et al., 2001; Lewis et al., 2003; Pierce et al., $775,00 per year if lost labor costs are factored in. Given that 2004). At the state level, Florida’s recent reinvigoration of the significant revenue losses associated with ciguatera continue to HAB and Red Tide State Task Forces has led to an increasing exist for fish dealers who produce grouper on Florida’s east coast scientific, management and public focus on HAB mitigation (Raizin and Meaburn, 1988), these estimates are likely low. In research and application within the state. Florida’s Red Tide the south Pacific region where it is endemic, ciguatera poisoning Mitigation and New Technology Initiative Program (2019–2025) has been shown to result in increases in health care costs (Lewis, also represents a substantial unique state effort to fund the 1986), labor productivity losses (Bagnis et al., 1992) and tourism development of new technology and mitigation research and (Lewis, 1992) and fish sale (Yeeting, 2009) losses ranging from application efforts related to K. brevis blooms. $1.1 million (Bagnis et al., 1992) to $22 million dollars annually (Hoagland et al., 2002). Other HABs, such as Synechococcus spp. blooms in Florida Bay, and cyanobacterial blooms statewide, FLORIDA HABs undoubtedly have significant negative impacts on both tourism and fisheries but economic losses have not yet been quantified. The state of Florida routinely monitors for more than 75 Management efforts are necessary to prevent or lessen HAB species in freshwater to marine environments. While the economic, environmental and human health impacts of HABs agencies directly involved are primarily Florida Fish and Wildlife and these generally focus on HAB mitigation. Mitigation of Conservation Commission’s Fish and Wildlife Research Institute HABs is comprised of 3 categories: prevention of HABs, control for estuarine and marine HABs and the Florida Department of HABs and associated toxins and mitigation of the impacts of Environmental Protection for freshwater HABS, many local of HABs (Boesch et al., 1996; CENR, 2000; Sengco, 2009a,b). municipalities and counties, especially those in southwest Prevention focuses on strategies to prevent bloom occurrence Florida that experience annual K. brevis blooms, maintain some or to limit their scope. These include limiting nutrient supply monitoring and management capabilities, especially with beach to blooms, management of the physical conditions that play cleanups, or directly collaborate with the state agencies. The a role in initiation and preventing HAB introductions to new following sections summarize the main Florida HAB species of areas (Anderson, 2004) and requires critical knowledge of concern for human, environment and economic health in the the biological, chemical and physical factors contributing to state. It is by no means an exhaustive list, but is meant to provide bloom initiation which may not be known. Control strategies a summary of the relevant state of knowledge of each HAB focus on efforts to destroy or remove both the HAB cells species to allow evaluation of the potential risks associated with and associated toxins and include both application of chemical each, especially in light of Florida’s ongoing demographic and controls [e.g., copper sulfate (Sengco, 2009b) and removal environmental challenges. technologies (Hallegraeff et al., 2017)]. Mitigation has received the greatest scientific and funding focus with both HABs in Dinoflagellate HAB Species general and with Florida HABs, especially K. brevis blooms, Karenia brevis (Florida Red Tide) and includes efforts to limit the impact of blooms through Blooms of the toxic dinoflagellate Karenia brevis represent monitoring, education and communication outreach (Kleindinst perhaps the most widely known and potentially greatest HAB and Anderson, 2004; Fleming et al., 2007; Kirkpatrick et al., 2008; threat to the state. Known colloquially as Florida Red Tide, Nierenberg et al., 2011) as well as development and application of these blooms reoccur annually in southwest Florida, impact the HAB forecasting models (Walsh et al., 2001; Stumpf et al., 2003, greatest number of people and biota both directly and indirectly, 2009; McGillicuddy, 2010; Kavanaugh et al., 2013). For HABs in and have the largest, most widespread economic impacts Florida, monitoring related technologies are rapidly advancing of all Florida HABs (Heil and Steidinger, 2009; Steidinger, and being applied, from molecular and optical detection methods 2009). Considered among the most predictable of global HABs, (e.g., HABscope for K. brevis monitoring, Hardison et al., K. brevis (formerly Gymnodinium breve, Ptychodiscus brevis, and 2019) to improved impact predictions (e.g., NOAA respiratory Gymnodinium brevis) blooms have a long and extensive history predictions, Stumpf, 2008). which predates the taxonomic identification and description of Florida has perhaps the earliest attempt to mitigate the the causative dinoflagellate after one of the most destructive risks associated with a marine HAB when in 1947, during one blooms on record in 1947 (Davis, 1948). Galtsoff (1948) reported of the most severe K. brevis blooms on record in southwest of the 1947 bloom that ‘All the beaches in the Fort Myers area Florida, Florida Senator Claude Pepper requested that the became littered with dead (fish) bodies which were reported to Frontiers in Ecology and Evolution | www.frontiersin.org 7 June 2021 | Volume 9 | Article 646080
Heil and Muni-Morgan Escalating HAB Risks in Florida
accumulate at a rate of more than 100 pounds per linear foot of oceanography of this region as well as the coastal morphometry.
shore line.’ But the existence of K. brevis blooms is known to Vargo (2009) reviewed the 24 theories proposed to explain
predate this 1947 bloom based on records of its unique human K. brevis blooms from the 1880’s to 2009. Many early red
symptomology (Steidinger, 2009). Respiratory irritation, which tide studies attempted to associate coastal blooms with local
occurs in humans exposed to aerosolized brevetoxins at or near nutrient, weather or physical conditions. Ingle and Martin (1971)
bloom impacted beaches or in the vicinity of blooms offshore, attempted to correlate bloom occurrence with an Iron-index of
was first noted in 1917 (Taylor, 1917). The unique human riverine conditions while Slobodkin (1953) related blooms to
symptomology of Neurotoxic Shellfish Poisoning (NSP), the low salinity, coastal water masses. Even in the 1950’s controversy
syndrome associated with consumption of shellfish exposed to existed surrounding the role of local nutrient inputs such as
K. brevis which have concentrated brevetoxins, was noted in 1880 the Caloosahatchee River on blooms, with Murdock (1954)
in Tampa Bay in association with local oyster saloons (Steidinger, arguing that ‘The continuing high rate of water release from the
2009). K. brevis bloom history likely extends much further back Caloosahatchee River may be a contributing cause to Red Tide
in GoM history based on anecdotal reports and ship logs which Outbreaks,’ while Graham et al. (1954) pointed out that ‘Neither
describe extensive fish kills in the region (Steidinger, 2009). the rivers, nor the bottom of the Gulf, nor the deep water of the
The more recent record of K. brevis blooms has received Gulf can be held as a source of phosphorus sufficient to increase
much public attention. With the onset of formal state red tide the concentration in the body of coastal water to the values which
monitoring in the 1980’s and the establishment of an extensive are found in red tide samples.’ None of these studies successfully
monitoring network, the recent bloom record is extensive, with explained how an organism characterized by relatively slow
well documented blooms of varying extent, duration and impacts growth rates, 0.2–0.3 divisions day−1 (Vargo, 2009), was able
occurring almost annually. The state HAB Historical Database to dominate phytoplankton biomass in these coastal blooms so
of Florida currently includes >85,000 georeferenced entries for rapidly until Steidinger (1975) recognized and documented the
K. brevis concentrations dating from 1952 to current times, and four stages of K. brevis blooms: initiation, growth, maintenance
was originally compiled in 2000 from more than 70 different and termination. Blooms initiate 18–74 km offshore in 12–
entities and sources (e.g., academia, non-profit, local state, 37 m depths on the mid-shelf of the southwest Florida coast,
and federal agencies) (Haverkamp et al., 2004). This database most often between Tarpon Springs and Naples (Steidinger,
reflects the temporal, spatial and depth biases associated with 1973). While offshore initiation has been documented in 1966,
these disparate data sources and the event response nature of 1976, 1979, 1985, 1998, and 2008 (Steidinger, 2009; Heil et al.,
K. brevis sampling prior to formal monitoring efforts in the 2014a), identifying this stage remains problematic due to the low
1990’s. Although Brand and Compton (2007) have interpreted concentrations of subsurface K. brevis cells which are difficult to
the database as supporting an increasing frequency of K. brevis detect, either remotely or with autonomous technology, and the
blooms in southwest Florida, statistical analysis of the database large potential offshore geographical area over which the blooms
for long term trends remains problematic (Heil et al., 2014a). potentially initiate. At this stage, physical drivers are crucial to
Walsh et al. (2006) examined the long term records of K. brevis bloom development. Offshore upwelling related to Loop Current
blooms off both Texas and southwest Florida in conjunction intrusion plays an important role in bloom initiation, with some
with available nutrient data and concluded that while increasing upwelling required for initiation (Liu et al., 2012; Weisberg
incidences of blooms off Texas were likely related to nutrient et al., 2014). Too much upwelling, however, delivers sufficient
discharges from the Mississippi River, those off Florida were upwelled NO3 − to the shelf bottom waters to favor diatom
not directly related to nearshore nutrient inputs. Regardless of development and impede K. brevis growth (Heil et al., 2001;
prior bloom history, however, coastal development continues, as Weisberg et al., 2016). Cells then grow slowly and are transported
does ongoing immigration to the state and the eutrophication of cross-shelf via the bottom Ekman layer (Weisberg et al., 2009,
Florida’s freshwater, estuarine and coastal waters. The net effect 2016), driven by wind-driven and upwelling-related transport.
of this is that more Florida residents and visitors are experiencing Winds, frontal systems and longshore currents act to concentrate
and being exposed to Florida Red Tide and its environmental and increasingly dense K. brevis populations shoreward (Tester and
economic impacts over time than ever before. Steidinger, 1997; Vargo et al., 2001, 2004; Weisberg and He, 2003;
Karenia brevis cells are a natural feature of the GoM and Janowitz and Kamykowski, 2006) where the blooms may persist
cells are found year round throughout the GoM at background for months to years (Steidinger, 2009). Weisberg et al. (2019)
concentrations of 1,000 cells L−1 or less (Geesey and Tester, demonstrated that the dramatic increase in cell counts off the
1993). Although blooms occur throughout Florida coastal waters, Pinellas County coastline in September 2018 which contributed
including the Panhandle and the east coast, blooms in these to the unusually severe 2017–2019 K. brevis bloom was shown to
regions are preceded by established blooms in southwest Florida be due to advection from the offshore formative region (Weisberg
waters in the region between Tarpon Springs and Naples (Heil et al., 2019). This 2018 southwest Florida bloom was subsequently
and Steidinger, 2009; Steidinger, 2009). In this southwest region advected to the Florida Panhandle and east coast in a similar
blooms occur almost annually, initiating in late summer to early manner later in the bloom as has been demonstrated for K. brevis
fall and lasting anywhere from 3 to 4 months to greater than blooms in 2005 (Carlson and Clarke, 2009).
30 months in 1994–1997. The nutrient sources that sustain K. brevis blooms as well as
To understand why blooms are most common in southwest the nutrient physiology of K. brevis are complex. Trichodesmium
Florida, there is a need to understand the physical and chemical blooms have long been observed to immediately precede and
Frontiers in Ecology and Evolution | www.frontiersin.org 8 June 2021 | Volume 9 | Article 646080Heil and Muni-Morgan Escalating HAB Risks in Florida
often co-occur with K. brevis blooms on the west Florida mouth can utilize some fraction of inland agricultural nutrient
shelf and a relationship between the two species was suggested sources. Uhlenbrock (2009) examined nutrient concentrations
(Chew, 1955; Steidinger, 1973; Taylor and Pollingher, 1987). within the river during 2005 releases and concluded that
Walsh and Steidinger (2001) documented their co-occurrence nutrient loading rates into San Carlos Bay from the River
over a 41 year period on the west Florida shelf from 1957 to provided sufficient DON and DIN to support the K. brevis
1998 and hypothesized that these two species were nutritionally bloom at the river mouth during the study. Note that these
linked through the transport and deposition of Fe-rich Aeolian blooms often extend well to the south and north of the
dust from north Africa, which supplied the Fe required for river mouth, and when the larger bloom areas are taken
Trichodesmium N2 fixation. Lenes et al. (2001) documented into account, there are insufficient nutrient inputs from the
increases in Fe concentrations in surface water after dust Caloosahatchee River to support the larger blooms. Heil et al.
deposition, with subsequent increases in DON and K. brevis (2014c) utilized nutrient stoichiometry to examine the potential
concentrations. Trichodesmium can release up to 50% of fixed N role of Caloosahatchee River N and P loading rates, in
to the environment as NH4 + and dissolved organic N (Capone comparison with other known nutrient sources for blooms,
et al., 1994; Glibert and Bronk, 1994). This N, in turn, is taken up to support small, medium and large estuarine, coastal and
by K. brevis (e.g., Lenes et al., 2001; Mulholland et al., 2002, 2006, offshore K. brevis blooms. River inputs were significant for small
2014; Sipler et al., 2013; Heil et al., 2014c; Killberg-Thoreson et al., estuarine blooms at the river mouth but decreased significantly
2014). for larger estuarine blooms and small coastal blooms. These
As blooms grow and are transported nearshore, the nutrient results suggest that the input of river N and P, while significant
sources available to cells increase and can include (1) benthic for smaller K. brevis blooms at or near the river mouth, are
nutrient flux (Dixon et al., 2014a); (2) photochemical nutrient insufficient to account for blooms of higher concentrations or
production (Bronk et al., 2014); (3) nitrification (Bronk et al., larger spatial extent.
2014), (4) zooplankton grazing (Walsh and O’Neil, 2014); and The mechanisms controlling bloom termination likely include
(5) nearshore coastal sources from estuarine and river runoff physical, chemical and biological processes. Blooms may
and inputs (Vargo et al., 2008; Dixon et al., 2014b; Heil be transported offshore, entrained in offshore fronts, and
et al., 2014c). As bloom concentrations increase nearshore to transported out of the area (Steidinger, 2009). Blooms frequently
concentrations >106 cells L−1 (Heil and Steidinger, 2009), transport south to the Ten Thousand Island area in southwest
nutrient regeneration from dead fish also can play an increasingly Florida, then migrate either east through the Florida Straits and
important role (Walsh et al., 2009; Killberg-Thoreson et al., up the east coast (15 times from 1972 to 2018) or westward into
2014; Heil et al., 2014c). The exact sources which contribute the central Gulf. Chemical and biological factors may include
to bloom maintenance nearshore depends upon bloom latitude nutrient impoverishment as well as bacterial and viral processes.
as well as distance offshore and bloom age (Heil et al., 2014a). Lenes et al. (2013), in a bloom simulation which examined
Nutrient stoichiometry calculations (Vargo et al., 2008; Heil et al., factors important in K. brevis bloom termination, reported a
2014c) have shown that sufficient nutrients are present to support modeling efficiency of 0.68 when a bacterial lysis term was
moderately sized, nearshore K. brevis blooms, during average introduced to nutrient limited K. brevis populations. Algicidal
estuarine flow years: combined estuarine sources contribute up bacteria (Mayali and Doucette, 2002; Roth et al., 2007, 2008)
to 17 and 69% of the N and P needs of these blooms, although as well as viruses (Paul et al., 2002) have been documented
only N2 fixation and release and decay of seasonal Trichodesmium for K. brevis, but their role in bloom dynamics and bloom
bloom biomass are sufficient to provide for the N needs of larger termination is unknown.
blooms (Lenes and Heil, 2010). Vargo (2009) summarized the physiological and ecological
The factors that control K. brevis bloom expansion and characteristics of K. brevis that contributes to its dominance of
termination are less understood. Favorable physical and sufficient coastal phytoplankton communities during blooms. Cell motility
nutrient sources are required to expand blooms and increase may play a role, as K. brevis is capable of complex physiological
their biomass. Potential nutrient sources that are important regulation of its position in the water column (Heil, 1986;
to these bloom stages may include additional nutrient sources Kamykowski et al., 1998; Sinclair and Kamykowski, 2008; Heil
derived from excessive freshwater inputs linked to hurricanes et al., 2014b) as well as an effective photoadaptive strategy
or water management practices. Hu et al. (2006) suggested (Shanley, 1985; Shanley and Vargo, 1993; Millie et al., 1997;
that a series of hurricane inputs in 2004 contributed to the Evens et al., 2001; Evens and Leblond, 2004). Karenia brevis
severity of the 2005 K. brevis bloom. The severe 2017–2019 may gain a competitive advantage through the production of
bloom was preceded by intense flooding and runoff following allelopathic substances (Kubanek et al., 2005; Prince et al.,
Hurricane Irma in fall of 2017, along with an extremely 2008, 2010; Poulson-Ellestad et al., 2014; Poulin et al., 2018)
wet season in 2018 which resulted in management decisions and a reduction in grazing losses due to the negative impacts
to release high volumes of nutrient-laden Lake Okeechobee of brevetoxins on higher trophic levels (Huntley et al., 1986;
water through the Caloosahatchee and St. Lucie Rivers. Both Turner and Tester, 1989, 1997; Lester, 2005; Waggett et al.,
a δ15 Nparticulate value at the Caloosahatchee River mouth 2012; Walsh and O’Neil, 2014). Not only is K. brevis able
(Yentsch et al., 2008) and statistical tests with convergent cross to utilize a variety of different nutrient sources, but nutrient
mapping and upriver N concentrations (Medina et al., 2020) physiology of K. brevis may also play a significant role in
suggest that K. brevis blooms at the Caloosahatchee River the dominance of these blooms. Recent evidence suggests that
Frontiers in Ecology and Evolution | www.frontiersin.org 9 June 2021 | Volume 9 | Article 646080Heil and Muni-Morgan Escalating HAB Risks in Florida K. brevis may also be capable of mixotrophic uptake of the to different trophic levels. However, Flewelling et al. (2005) picocyanobacteria Synechococcus (Jeong et al., 2005; Glibert et al., reported elevated brevetoxin levels in the tissue of live fish 2009a; Procise, 2012). Growth of marine picocyanobacteria in collected from the wild as well as in whole fish contained in southwest Florida coastal waters is correlated with urea (Heil the stomachs of dolphins (Tursiops truncatus) killed in a marine et al., 2007), which has been shown to increase with both mammal mass mortality in the Florida Panhandle in 2004. large scale hurricane related inputs (Heil et al., 2007) and Additionally, Naar et al. (2007) demonstrated that brevetoxins localized episodic, wind driven inputs (Ivey et al., 2020). Nutrient can accumulate in both omnivorous and planktivorous fish stoichiometry also may play a further role in K. brevis blooms by dietary transfer in both the laboratory and in the natural as Walsh et al. (2006) suggested that the generally low DIN:DIP environment and persist for up to a year after the bloom ratios that characterize southwest Florida rivers (
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